ECOHAB 2015: Project Summaries

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Integrating Cell and Toxin Cycles of Karlodinium veneficum with Key Environmental Regulators: In Situ Studies of Predictive Determinants for Bloom Toxicity

Institutions:  University of North Carolina at Charlotte, University of Maryland Center for Environmental Science

Investigators: Matthew W. Parrow (lead), Allen R. Place

The dinoflagellate Karlodinium veneficum blooms along Mid-Atlantic coasts and produces structurally characterized, quantifiable toxins called karlotoxins (KmTX) that kill fish and exhibit widespread toxicity to other organisms.  However, toxicity varies widely among different bloom populations, and within populations over time. Coastal management requires knowledge and tools to better predict how, when, and why K. veneficum cells (and thus blooms) become highly toxic.  Our recent research has demonstrated that karlotoxins increase significantly in stationary phase cultures, particularly under growth-limiting conditions caused  by low N, P, or selenium (Se).  These and other results strongly suggest a simple but strongly predictive inverse relationship between the rate of cell proliferation and cellular toxin quotas in K. veneficum populations.  Furthermore, it has been recently found that karlotoxin production is light-dependant with a diel biosynthetic cycle that closely corresponds to the cell cycle.

The objective of this project is to quantify the relationship between K. veneficum cell proliferation rates and toxicity in cultures and natural blooms by correlating the diel cell cycle, in situ growth rates, and cellular karlotoxin accumulation in relation to key environmental factors identified as primary growth/toxicity determinants of K. veneficum. The overall hypothesis is that growth-limited (slowly or non-proliferating) K. veneficum cells in both culture and field blooms will arrest in G1 for multiple L/D cycles, undergo several cycles of karlotoxin synthesis, and become significantly more toxic.  Put simply, rapidly proliferating cells have a low toxin content whereas slowly or non-proliferating cells accumulate toxin and become more toxic.

The experimental approach will be to examine cultures (Year 1) and natural blooms (Years 2 & 3) of K. veneficum for cell cycle progression, in situ growth, and karlotoxin accumulation over time and in relation to key environmental factors using digital microfluorometry and LC-mass spectrometry.  Year 1 experiments will consist of laboratory range-finding studies and Year 2 & 3 experiments will consist of intensive bloom sampling and mesocosm experiments in the Baltimore Harbor where blooms of toxic K. veneficum are an annual phenomenon. This research will provide novel information on how K. veneficum in situ growth rates and toxicity are related and integrated with environmental factors, concepts which are critically needed to validate predictive models to forecast bloom growth and toxicity.

Expected outcomes include adoption by area managers of information and techniques leading to better prediction of bloom toxicity, and improved quantitative understanding of the role of in situ population dynamics in K. veneficum bloom toxicity and ecology.


Interannual variability of PSP toxicity in eastern Maine: testing the leaky gyre hypothesis and improving regional forecasts and management

Institutions:  Woods Hole Oceanographic Institution, University of Maine, North Carolina State University, NOAA/NOS, NOAA/NMFS, Department of Fisheries and Oceans, Canada.

Investigators:  Donald M. Anderson (Lead), Dennis J. McGillicuddy,  Bruce A. Keafer, David W.Townsend, Ruoying He, Richard P. Stumpf, James P. Manning, Jennifer L. Martin

The Gulf of Maine (GOM) is a large continental shelf sea with extensive shellfish resources that are annually impacted by Alexandrium fundyense blooms and outbreaks of paralytic shellfish poisoning (PSP), leading to significant social and economic impacts every year, often totaling tens of millions of dollars in losses and sometimes more. Toxicity occurs in three main regions of the Gulf (the eastern and western Gulf of Maine (EGOM and WGOM), and Georges Bank) that are interconnected, but that can also behave independently due to large- scale oceanographic forcings. These areas have been the subject of past NOAA-funded investigations that have been highly productive in terms of scientific advances, publications, and management tools, but EGOM toxicity remains poorly understood, despite the serious nature of the PSP problem in that region and its hydrographic connections to the west. One major development from prior research programs is an A. fundyense population dynamics model that has been used to produce near-real-time weekly nowcasts and forecasts, and seasonal forecasts. That model is being transitioned for operational use by NOAA. Model skill is strongest in the WGOM where A. fundyense cyst abundance in a “seedbed” or accumulation zone off mid-coast Maine has proven to be a primary driver of interannual PSP variability. Skill is weakest in the EGOM because the mechanisms responsible for interannual variability are not thought to relate to cyst abundances in that subregion, which are very low, but instead to the advection of established vegetative A. fundyense populations that originate in the Bay of Fundy (BOF) where there is a major cyst seedbed and a gyre that can be retentive for A. fundyense cells.

We hypothesize that interannual variations in EGOM toxicity are controlled by these upstream populations, for which there are two key sources of variability: (1) growing conditions, and (2) hydrodynamic leakiness of the BOF gyre. Neither of these aspects is adequately represented in existing models. We therefore propose to investigate linkages between BOF A. fundyense populations and PSP toxicity in the nearshore and offshore waters of the EGOM, to characterize the physical mechanisms that control that export, and to use this information to improve regional HAB management, modeling, and forecasting.Recognizing that high-frequency in situ observations of A. fundyense concentrations in the two exit pathways from the BOF (either side of Grand Manan Island; Fig. 1) are needed to capture the episodic nature of the export process, we will utilize a network of novel biosensors called Environmental Sample Processors (ESPs) to obtain data that would not be feasible with ship-based surveys.

Daily autonomous measurements at multiple locations will be augmented by satellite-tracked surface drifters released within the gyre, and by three targeted survey cruises to provide spatial context for the ESP observations. Measurements of nutrients and water column structure from NERACOOS ocean-observing buoys will also be obtained. All of this information will be incorporated into our existing regional Alexandrium model and hindcast simulations run to identify mechanisms underlying patterns in EGOM shellfish toxicity.

The project team has extensive experience in all aspects of the proposed work, and has strong ties to managers and other stakeholders in the region. Furthermore, the project leverages a huge amount of ongoing activities and equipment –ESPs, mooring hardware, and contextual sensors that are owned by the PI, ship time, deployment and operational costs for a full field season, as well as ship of opportunity survey cruises and nearly a dozen soon-to-be-deployed nutrient sensors supported by the IOOS program – all at no cost to the program. This proposal is an important and timely opportunity to advance novel HAB biosensor technology while addressing a critical scientific question underlying regional toxicity in a highly productive and important shell fishing region. This effort is also directly responsive to the priorities of the ECOHAB program and of the NOAA Next Generation Strategic Plan.


Climate change impacts on the physiology and trophic dynamics of harmful algal species from Delaware’s inland bays.

Institution: University of Delaware

Investigators: Mark E. Warner (lead), Kathryn J. Coyne, Jonathan H. Cohen

Global climate change is expected to have profound impacts on biogeochemistry, nutrient cycling and biological process in the ocean, and species inhabiting coastal ecosystems are among the most vulnerable to these changes. Examining the effects of climate change on isolated species, however, will not adequately portray the extent of these impacts on complex biological communities. Previous research shows that elevated temperature and/or CO2 alters toxicity for some HAB species, but the consequences of altered toxicity on community dynamics and trophic interactions have not been investigated. Likewise, prior ECOHAB-funded research by Warner and Coyne investigating the effects of climate change on growth, physiology and expression of enzymes involved in C and N metabolism for local HAB species show species-  and strain-specific responses to changes in temperature and/or CO2. Results of this investigation also indicate substantial changes in nutrient quotas and partitioning of carbon biomass for some HAB species, even when no changes in growth rate were observed. Such shifts will likely alter the nutritional quality and mass transfer efficiency to grazers in a species-specific manner, possibly impacting zooplankton survival, growth and production rates.

The goals of this project are to investigate the effects of climate change on HAB species and the consequences of altered toxicity and nutritional quality of HAB species on micro- and mesozooplankton grazers. The interactive effects of temperature and CO2 on metabolism, resource partitioning, and toxicity in two raphidophytes (Heterosigma akashiwo and Chattonella subsalsa) and a dinoflagellate species (Karlodinium veneficum) will be examined under nutrient- replete or nutrient-limited conditions. Responses of the cultured micrograzers Oxyrrhis marina, Favella sp., and Strombidinopsis acuminatum, and the model copepod, Acartia tonsa, to climate change conditions will also be assessed. Once acclimated to CO2 and temperature levels expected at the end of this century, their ability to graze the target HAB species compared to non-harmful species cultured under the same conditions will be examined. The relative effects of toxicity, starvation and possible changes in algal fatty acid content on micrograzers and copepod grazing and egg production will be evaluated under both ambient and climate change-driven growth conditions. Behavioral changes and other sub-lethal effects on zooplankton reproductive output as a result of either toxicity or starvation will be evaluated. The possibility for direct and indirect trophic interactions between a target alga, micro- and mesograzer exposed to the same conditions will also be evaluated. Results of this project will lead to a better understanding of how changes in growth, toxicity and nutritional quality of HAB species will impact competitive and trophic dynamics in coastal ecosystems of the future.


Resolving the effects of resource availability, predation, and competition on brown tide dynamics via metatranscriptomics

Institutions:  Stony Brook University, Columbia University

Investigators:  Christopher J. Gobler (lead), Sonya Dyhrman

Aureococcus anophagefferens is a pelagophyte that causes harmful brown tides that have decimated multiple fisheries and seagrass beds in mid-Atlantic US estuaries for three decades. The recent sequencing of the Aureococcus genome, combined with comparative genomic studies, in situ ecosystem observations, and experimental studies have collectively evidenced the importance of multiple bottom-up and top-down controls of brown tides. While advances have been made in understanding how nitrogen impacts the occurrence of brown tides, the relative importance of other factors that strongly influence the onset of these HABs is unclear. Taking advantage of the Aureococcus genome sequence, on-going gene expression studies by the PIs, and advances in both high throughput sequencing and informatics technology, we propose a combined field and laboratory study using eco-transcriptomics to address the question: what are the precise environmental factors that drive the initiation, persistence, and demise of brown tides? We will generate transcriptomes (global gene expression patterns) for Aureococcus cultures exposed to a suite of environmentally conditions relevant to bloom formation including growth on multiple sources of organic matter, exposure to multiple types of zooplankton, selenium limitation, and ideal conditions. These transcriptomes will be used in conjunction with others the PIs have generated during prior projects (low nitrogen, low phosphorus, low light) to define precise transcriptomic signatures elicited by these factors. In the field, we will perform metatranscriptomic profiling of Aureococcus and competing phytoplankton populations in a chronically brown tide-prone embayment during the initiation, persistence, and decline of blooms while concurrently measuring pertinent environmental variables. We will perform incubation experiments during which we will perturb existing environmental conditions (nutrients, organic matter, light, grazing) to affirm factors that drive patterns of gene expression in, and dominance among, Aureococcus and competing phytoplankton species. The ability to quantitatively compare the specific transcriptomic profile of Aureococcus under multiple controlled laboratory conditions to the profiles of brown tides as they develop will identify the environmental factors that have the strongest influence on the growth and physiology of Aureococcus and competing phytoplankton during blooms. Assessing environmental conditions in concert with meta-transcriptomes over the course of brown tides will be the crux of our eco-transcriptomic approach: linking of expression of genes by a HAB and competing phytoplankton to specific environmental conditions to define the precise niche of each algal species. This approach will, therefore, provide a comprehensive understanding of the interaction of brown tides and their environment. Since most of the environmental conditions we will explore have been anthropogenically created (e.g. high N, high P, high organic matter, high metals, low light), our findings will support managerial actions to ameliorate blooms via the improvement of specific environmental conditions. Towards this end, we will host local and regional workshops with managers from NY State and the mid-Atlantic region to communicate the  results  of  this  project  with  the  ultimate  goal  of  providing  information  regarding environmental conditions that should be improved to manage and mitigate brown tides.


Last updated: July 11, 2016